Abstract

Sensory experience is necessary for the development of some receptive field properties of neurons in primary sensory cortical areas. However, it remains unclear whether the parameters of an individual animal's experience play an instructive role and influence the tuning parameters of cortical sensory neurons as selectivity emerges, or rather whether experience merely permits the completion of processes that are fully seeded at the onset of experience. Here we have examined whether the speed of visual stimuli that are presented to visually naive ferrets can influence the parameters of speed tuning and direction selectivity in cortical neurons. Visual experience is necessary for the development of direction selectivity in carnivores. If, during development, cortical neurons had the flexibility to choose from among different inputs with a range of spatial positions and temporal delays, then correlation-based plasticity mechanisms could instruct the precise spatiotemporal selectivity that underlies speed tuning and direction selectivity, and the parameters of an individual animal's experience would influence the tuning that emerges. Alternatively, the tuning parameters of these neurons may already be established at the onset of visual experience, and experience may merely permit the expression of this tuning. We found that providing different groups of animals with either slow (12.5 deg/s) or fast (50 deg/s) visual stimuli resulted in emergence of direction selectivity, but that speed tuning and direction selectivity were similar in the two groups. These results are more consistent with a permissive role for experience in the development of direction selectivity.SIGNIFICANCE STATEMENT The proper development of brain circuits and neural response properties depends on both nature (factors independent of experience) and nurture (factors dependent on experience). In this study, we examined whether the quality of visual experience of an individual animal influences the development of basic sensory detectors in primary visual cortex. We found that, although visual experience is required for the development of direction selectivity, tuning for stimulus speed could not be altered by specific experience with slow or fast stimuli. These results suggest that the tuning parameters for direction selectivity are specified independently of an animal's sensory experience, and that a range of experiences can promote the proper mature expression of direction selectivity in primary visual cortex.

Figures

Figure 1.

5

Hypotheses outline: models of the…

Figure 1.

13

Hypotheses outline: models of the development of direction selectivity in primary visual cortex.…

Figure 1.

Hypotheses outline: models of the development of direction selectivity in primary visual cortex. A, Two possible juvenile connection schemes between a group of LGN neurons that respond to combinations of 5 adjacent positions in space at 5 different latencies and a single V1 neuron. The single V1 neuron is illustrated only in the figure key above A. LGN neuron color key: red (strong) represents V1 connection exists and produces a strong response in the V1 neuron; gray (weak) represents V1 connection exists but only produces a weak response in the V1 neuron; white (not possible) represents V1 connection does not exist and cannot produce a response in the V1 neuron. B, Firing times of LGN neurons from A to a bar moving up and a bar moving down. LGN neurons with a strong connection to the V1 neuron cause a deflection in the V1 neuron's membrane potential that will lead to a spike if a threshold is crossed. C, Adult pattern of connections between LGN neurons and a single V1 neuron. D, Firing times of LGN neurons from C to a bar moving up and a bar moving down. The threshold for firing in the V1 neuron has increased from the juvenile state in B, and activity from multiple LGN neurons with strong connections is required for the V1 neuron to fire. The pattern of connections from LGN shown here results in the V1 neuron being selective for a bar moving down. E, F, If visual experience plays an instructive role in the development of direction selectivity, (E) we would expect training of Possible Juvenile State 1 with visual stimuli moving at fast and slow speeds to result in different patterns of connections between LGN and V1. F, Model responses of a V1 neuron to a bar moving up and a bar moving down for Juvenile State 1 before and after training with fast and slow speed visual stimuli. Before training, the cortical response largely reflects speed tuning of LGN cells. After training, the speed tuning is dominated by the pattern of connections. G, H, If visual experience plays a permissive role in the development of direction selectivity, (G) we would expect training of Possible Juvenile State 2 with visual stimuli moving at fast or slow speeds to result in identical patterns of connections between LGN and V1. H, Model responses to a bar moving up and a bar moving down for Juvenile State 2 before and after training with fast or slow speed visual stimuli. Speed tuning of the V1 neuron is dictated by constraints in the pattern of connections.

Experiment design. A, Electrophysiology setup. A 32-channel linear electrode array (NeuroNexus, A1x32-Poly2) is inserted into V1 of an anesthetized juvenile ferret (p31–p34). A receptive field center is found manually for placement of the visual stimulus monitor. Raw voltage data are recorded, and spike times are extracted for analysis. B, Time course of experiment. Experiment starts with a test phase to identify an optimal stimulus orientation at 25 deg/s (Stimulus 1) and response across a range of speeds to a bar moving bidirectionally in the two directions perpendicular to the optimal orientation (Stimulus 2). The test phase alternates for the duration of the experiment with one of three different 3 h visual training conditions: α, sinusoidal grating at optimal orientation moving bidirectionally at 12.5 deg/s; β, sinusoidal grating at optimal orientation moving bidirectionally at 50 deg/s; or γ, static gray screen control.

Figure 3.

5

Cortical cells respond best to…

Figure 3.

13

Cortical cells respond best to visual stimuli moving at 25 deg/s at a…

Figure 3.

Cortical cells respond best to visual stimuli moving at 25 deg/s at a particular orientation and direction of motion. Average responses (by animal) of V1 sites to Stimulus 1 (Fig. 2B) before and after 3, 6, and 9 h of training with one of the three training stimuli: (A) 12.5 deg/s, (B), 50 deg/s, and (C) control. Responses are normalized and aligned such that upward motion has the largest response. Black line indicates condition average. Gray lines indicate individual animal averages. Insets, Condition average polar plots with up being 90 degrees. Error bars indicate SEM across animals.

Cortical cells exhibit rapid increases in direction selectivity measured at 25 deg/s with either 12.5 or 50 deg/s training. A, E, Color indicates training condition: yellow represents 12.5 deg/s; green represents 50 deg/s; blue represents control. A, Average responses (by animal) of 1 − DCV at 25 deg/s for each of the three training conditions. Black line indicates estimate of rate of change in 1 − DCV over time and is reported as m in units of Δ1 − DCV/h. *p < .05 (Bootstrap test). B–D, Cumulative histograms of 1 − DCV for all sites for each of the three training conditions. V1 sites in animals that received training exhibited a progressive increase in direction selectivity, whereas V1 sites in control animals did not. E, Animal averages of 1 − CV for each of the three training conditions. Black line indicates estimate of rate of change in 1 − CV over time and is reported as m in units of Δ1 − CV/h. F–H, Cumulative histograms of 1 − CV for all sites for each of the three training conditions. (I) Animal averages of tuning width for each of the three training conditions. Black line represents estimate of rate of change of tuning width over time and is reported as m in units of degrees/hour. (J–L) Cumulative histograms of tuning width for all sites for each of the three training conditions.

Cortical cells exhibit rapid changes in direction selectivity across a consistent range of speeds with either 12.5 or 50 deg/s training. A–C, Condition average DSI values at each time point at three different test speeds: (A) 12.5 deg/s, (B) 25 deg/s, and (C) 50 deg/s. Error bars indicate SEM. Color indicates training condition: yellow represents 12.5 deg/s; green represents 50 deg/s; blue represents a static gray screen (control). Black line indicates estimate of average change in DSI over time and is reported as m in units of ΔDSI/h. *p < .05 (Bootstrap test). On average, cortical neurons acquired speed tuning preference for 25 and 50 deg/s regardless of the speed of the training stimulus. D, E, Condition median speed tuning, or speed that elicited the maximum response, in the preferred (D) and null (E) directions. Error bars indicate median average deviation. Training had no influence on speed tuning in either the preferred or null direction.

Figure 7.

5

Maximum stimulus-evoked response in the…

Figure 7.

13

Maximum stimulus-evoked response in the preferred and null directions, and spontaneous activity for…

Figure 7.

Maximum stimulus-evoked response in the preferred and null directions, and spontaneous activity for each of the three training conditions over time. A, B, Maximum firing rate in the preferred (A) and null (B) directions. C, Spontaneous activity. Error bars indicate at condition median value, and error bars indicate median absolute deviation. Points are individual animal median values. Black line indicates estimate of average change in firing rate over time and is reported as m in units of ΔHz/h. *p < .05 (Bootstrap test). Rate of change in response to the preferred and null direction was similar within training conditions. Training at 50 deg/s had a significantly different rate of change in firing rate (a decrease) in both the preferred and null directions compared with 12.5 deg/s training and control. There was no difference in rate of change of spontaneous activity between training conditions.